- Email: [email protected]
Removal of Epimacular Membranes
Removal of Epimacular Membranes RAYMOND R. MARGHERIO, MD, MORTON S. COX, Jr, MD, MICHAEL T. TRESE, MD, PATRICK L. MURPHY, MD, JILL JOHNSON, MD, LOUISE A. MINOR, PhD, MD
Abstract: Vitreous surgery was used to remove epiretinal macular membranes in 328 cases, 184 (56%) of which had membranes that were considered idiopathic and 144 (44%) which were due to other causes. The 12- to 92month follow-up showed that visual acuity improved two lines or more in 243 (74%) of the eyes, 79 (24%) were unchanged and 6 (2%) became worse. Recurrence of membranes was seen in 24 (7.3%) eyes and 27 (8%) eyes developed complications. In the idiopathic cases visual results were significantly better and complications fewer. Rapidly progressive nuclear sclerosis was noted in 23 (12.5%) eyes. The degree of cystoid edema had no relationship to the final visual result. Pseudoholes which were present in 14 (8%) of the idiopathic cases either became smaller or disappeared following successful surgery with an average increase in acuity of five lines. [Key words: cystoid macular edema, epiretinal macular membranes, macular cyst, macular pucker, preretinal macular fibrosis, primary retinal folds, pseudohole of the macula, surface wrinkling retinopathy, vitrectomy, vitreous surgery.] Ophthalmology 92:1075-1083, 1985
Cellular membranes on the inner retinal surface are common. They have occurred in 2 to 6% of autopsied eyes having an increasing incidence with age. 1•2 Most spontaneous or idiopathic membranes cause minor visual disturbances and are slowly progressive, while some membranes cause progressive metamorphopsia, Amsler grid distortion, and reduced visual acuity due to distortion and/or obscuration of the macula. The macular distortion produced by epiretinal membranes has been called primary retinal folds, macular pucker, preretinal macular fibrosis, surface wrinkling retinopathy, preretinal macular fibrosis, internal-retinal fibrosis, and cellophane maculopathy. The condition is commonly called a macular pucker when it follows the surgical reattachment of a rhegmatogenous retinal detachment. From the Division of Ophthalmology, Michigan State University, College of Human Medicine, East Lansing, Michigan, and the Department of Ophthalmology, William Beaumont Hospital, Royal Oak, Michigan. Presented at the Eighty-ninth Annual Meeting of the American Academy of Ophthalmology, Atlanta, Georgia, November 11-15, 1984. Reprint requests to Raymond R. Margherio, MD, 3535 W. 13 Mile Road, Suite 507, Royal Oak, Ml 48072.
In this series, the results of a long-term study of 328 affected eyes that have undergone vitrectomy with epiretinal membrane peeling will be reported. Of the 328 eyes, 184 were considered to be idiopathic or spontaneous, and although this series reports on all types of etiologically identified epiretinal macular membranes, particular emphasis is placed on idiopathic epiretinal membranes rather than macular puckers following retinal surgery. An attempt is made to identify some of the prognostic factors that may affect the selection of patients for possible surgical intervention, including thickness of membrane, presence of a visible edge, location of membrane, preoperative cystoid macular edema, and presence of a macular cyst or pseudohole. Surgical technique is discussed with comments regarding avoidance of complications and ways of dealing with unusual case types.
MATERIALS AND METHODS All patients were operated on by a member of Associated Retinal Consultants in Royal Oak, Michigan between April 1977 and October 1983. The patients were generally referred for evaluation with a diagnosis 1075
OPHTHALMOLOGY
•
AUGUST 1985
of macular degeneration. Eyes exhibiting epiretinal macular membranes were sub-classified based on presumed etiology. Eyes with any evidence of diabetic retinopathy, senile macular degeneration, glaucoma with field loss, previous retinal detachments involving the macula, or with significant opacities of the ocular media were excluded. A complete eye examination was performed on all eyes preoperatively. In addition, a comprehensive evaluation of the vitreous was performed with a contact lens. Stereo fundus photographs were taken and fluorescein angiography was performed when possible. In eyes with an apparent macular cyst, hole, or pseudohole, the "slit beam sign" 3 was used. In performing the slit beam test, a narrow beam of light is directed over the macula. The presence of a macular hole or large cyst causes the patient to report a discontinuous line or gap in the beam, whereas small cysts or pseudoholes cause the light to be pinched in appearance. Other lesions, such as detachments of the neurosensory retina, cause a bowing of the slit. In this study, a "positive" response was when a patient described the slit as being discontinuous. Eyes with positive "slit beam signs" were not considered favorable surgical candidates. Initially, no eye was considered for surgery with a corrected vision of better than 20/200. As the surgical technique was improved, and detailed analysis showed that the procedure was relatively safe and usually effective, this parameter was lowered to approximately 20/ 70 on selected patients. However, the vast majority of patients considered for surgery had corrected visual acuities that were less than 20/200. Many patients were seen with epiretinal macular membranes and visual acuities better than 20/70. These patients were given an Amsler grid and examined, generally, at six-month intervals. Statistical analyses were done using an Apple II C Computer Statistics Package. Two nonparametric tests were performed. The first was the Spearman rank-order coefficient rs (rho) which tests the relationships between two variables by assigning rank orders and then computing the differences between the ranks and squaring the differences (to eliminate signs). The second was the Kendall Tau (T) which looks at data by performing pairwise comparisons between one pair of values and all other lower ranking pairs.
SURGICAL OBJECTIVES AND TECHNIQUES The initial surgical objective in these cases was to perform a core vitrectomy, utilizing either a full function vitrector or divided system vitrectomy instrumentation. A bimanual technique was used for the membrane stripping, generally with a full function vitrectomy instrument entering the globe superior temporally and a bent needle superior nasally. A 23-gauge 1112 inch dis-
1076
•
VOLUME 92
•
NUMBER 8
posable needle attached to a tuberculin syringe filled with a balanced salt solution is most convenient for the procedure. Prior to bending, the needle is inserted into the vitreous cavity through the pars plana. Any sclera, etc., is then irrigated out of the bore and an appropriate bend is made near the tip under the microscope. The needle can then easily be reinserted into the globe through the self-sealing puncture wound, which can later be closed with a single suture. In cases where forceps or scissors may be required, this nasal inci!Sion is made with an appropriate knife or stylet. Approximately one-half of the eyes of this series were operated on with a full function instrument and one-half using a divided system. Prior to attempting the membrane peeling, the posterior one-half of the globe must be free of vitreous. This was easily accomplished in most of the eyes in this series with a posterior vitreous detachment present preoperatively. In the remainder of the eyes, without a posterior vitreous detachment, a complete posterior vitrectomy was necessary to remove all vitreous opacities, thereby improving visualization and reducing the possibility of peripheral vitreoretinal traction that could cause retinal tears or detachment. In performing the core vitrectomy, an attempt was made to leave as much vitreous between the core vitrectomy and the lens as possible in an attempt to reduce the possibility of trauma to the lens, and hopefully, the incidence of postoperative cataract formation. Following the core vitrectomy, a bent 23-gauge needle or vitreoretinal pick4 was used to strip away the epiretinal tissue in order to allow the retina to assume a more normal configuration. In a minority of cases the epiretinal tissue itself was opaque, causing additional interference with clear vision. The manner in which the core vitrectomy was achieved varied with each case, depending on multiple factors determined by careful preoperative evaluation. These factors included the presence of a lens or pseudophakos, previous retinal reattachment surgery, transvitreal bands, preexisting retinal tears or subclinical detachments, atrophic or nonprofused retina, presence of a macular cyst or pseudohole, and the clinical appearance and position of the epiretinal membrane. Of the aforementioned considerations, eyes with transvitreal membranes, usually associated with previous retinal detachments, were technically the most difficult. Also, eyes that had previous scleral buckling procedures with very high buckles had to be approached in such a way that the shafts of the instruments would pass from the pars plana to the paramacular region with enough clearance over the buckle to avoid tearing the retina during dissection. In cases where retinal tears or subclinical detachments were noted, the retinal repair was carried out at least three months prior to any attempt at vitrectomy and removal of surgical epiretinal membranes. There were no subsequent detachments in eyes treated in this fashion. In almost all cases the membrane itself was first
MARGHERIO,
et al •
dissected with a bent 23-gauge needle. If the membrane demonstrated an obvious edge this was dissected first. If not, the area of greatest apparent thickness or tortuosity was dissected using the sharp point of the needle over one of the minor retinal vessels in an attempt to find an edge. When using this technique, a small intraretinal bleed was noted before a full thickness perforation occurred during the dissection. In cases where there was no edge, obvious thickening, or epicenter, the same technique was used in multiple areas until an edge was encountered, which then allowed successful stripping of the membrane. In cases where atrophic retina, due to trauma or vascular occlusive disease, etc., was identified, more care was necessary in all phases of the membrane stripping, since these retinas did not exhibit the same amount of tensile strength and were more apt to tear with the membrane stripping than a retina not so compromised. Special care was taken when stripping the membrane over the macula, especially in cases where there was a pseudohole or cyst in order to avoid creating a lamellar or true macular hole. This complication was not encountered in this series, but has been seen in several eyes undergoing membrane stripping for diabetic retinopathy. In most cases, the membrane was removed starting from an area two to three disc diameters temporal to the macula and proceeding towards the disc nasally and the arcades inferiorly and superiorly, removing as much intact membrane as possible. In cases where a specimen was desired for histopathologic study or where the edge of the membrane could not be grasped with the needle for dissection, intravitreal forceps were used. Care was taken during the dissection phase to observe all areas of potential traction so that retinal tears were not created. In some cases the membrane peeled and became very extensive, going far beyond the arcades. In these cases it was very difficult to observe all areas of traction and it was felt these membranes should be cut circumferentially with intravitreal scissors to reduce the possibility of retinal tears and/or detachment. In peeling almost all cases of idiopathic membranes, which were generally thin and transparent, the bent 23-gauge needl~ was the instrument of choice. Where thick, however, opaque membranes were encountered with large convolutions of retina, a vitreoretinal pick with a more blunt tip was useful to separate the membrane from the retina and was less likely to cause a retinal break especially in some cases of macular pucker after a scleral buckling procedure where often a "plug" of fibrous material had to be removed from the "epicenter" of the pucker if visual improvement was to occur. With thin transparent membranes there is generally no need to search for multiple layered membranes. However, with thicker, more opaque membranes there are often multiple layers that must be sequentially peeled in order to obtain the desired end point. In most instances, by using the previously noted technique of careful dissection over small vessels until encountering capillary bleeding, incomplete removal of multilayered
EPIMACULAR MEMBRANES
Table 1. Age Distribution in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Idiopathic Cases
Other
All
21-86 67.8
5-83 54.3 57
5-86 60.67 65
Range (years) Mean (years) Median (years)
69
membranes can be avoided. However, since the eyes that had an air-fluid exchange were not selected in a randomized fashion, a statistical analysis of the effects on final visual outcome was not significant. Any retinal tears created during the vitrectomy or stripping were treated with trans-scleral cryopexy, transvitreal cryopexy, or photocoagulation. In cases where there was a great deal of folding of the retina, it was felt that an air-fluid exchange and postoperative prone positioning of the patient might result in a better anatomic result. This was done in approximately one-half of the cases in this series.
RESULTS The age of the patients in this study ranged from 5 to 86 years (mean, 60.67 years) (Table 1). The idiopathic group were generally older with a mean of 67.8 years, which would be consistent with the findings of Foos and others 1•2 regarding incidence, etc. There were 140 males and 188 females, with a marked prevalence of females in the idiopathic group and a slight prevalence of males in the other category (Table 2). The most common type of macular membrane was spontaneous or idiopathic. Membranes following retinal reattachment were the second most common type. The membranes were also seen following the prophylactic treatment of retinal breaks, trauma, ocular inflammation and retinal vascular diseases. Two membranes were considered to be congenital in origin and one was associated with juvenile sex-linked retinoschisis (Table 3). The follow-up period after the removal of the epiretinal macular membranes from the 328 eyes ranged from 12 months to 92 months (mean, 41.2 months). The best preoperative visual acuity was 20/60. In most eyes the Table 2. Sex Distribution in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Idiopathic Cases
All
Other
No.
(%)
No.
(%)
No.
(%)
Male Female
63 121
(34) (66)
77
67
(53) (47)
140 188
(43) (57)
Total
184
(100)
144
(100)
328
(100)
1077
OPHTHALMOLOGY
•
AUGUST 1985
•
VOLUME 92
Condition
No.
(%)
Idiopathic Post-retinal detachment Retinal vascular Trauma Post-cryopexy, photocoagulation, etc. Inflammatory Congenital Congenital hereditary retinoschisis
184 95 13 12 11 10 2 1
(56) (29) (4) (4) (3) (3) (0.7) (0.3)
Idiopathic Cases
preoperative visual acuity was 20/200 or worse (Table 4). Economically useful vision (20/50 or better) was restored in approximately one-third (34%) of the operated eyes (Table 5). Forty-four percent of the eyes with idiopathic membranes achieved a visual acuity of 20/50 or better. Similar visual results were obtained in only 23% of eyes with membranes due to other causes. The average number oflines of improvement of visual acuity following macular membrane peeling was 3.45. The results again being better in the idiopathic cases (4.03 lines) versus the other cases (2.99 lines). Over all the visual acuity improved two lines or more in approximately 74% of the operated eyes. Twenty-four percent were unchanged and visual acuity was worse in 2% of the 328 eyes operated (Table 6). Twenty-seven eyes developed complications following surgery. The vast majority of these complications related to the recurrence of a retinal detachment in eyes with scleral buckles in place. These were all successfully repaired. The one case of endophthalmitis was also successfully treated. In the series of idiopathic cases the~e was a complication rate of approximately 2%, wh1ch was much lower than the overall complication rate of 8% (Table 7). Recurrence of epiretinal membranes was observed in 24 (7.3%) eyes. Recurrence was relatively infrequent except in younger patients and in eyes with membranes associated with retinovascular conditions (31% ), inflammation (20%) and trauma ( 17%) (Table 8). Table 4. Visual Acuity in 328 Consecutive Cases of Vitrectomy for Ep1ret1nal Macular Membrane Prior to Membrane Peeling
Visual Acuity 20/20-20/30 20/40-20/50 20/60-20/70 20/80-20/100 20/200 or worse Total
1078
No.
(%)
No.
(%)
(%)
(2 (15) (83) (100)
7 43 134
(4) (23) (73)
5 139
(3) (97)
7 48 273
184
(100)
144
(100)
328
All
No.
(%)
No.
(%)
No.
(%)
20/20-20/30 20/40-20/50 20/60-20/70 20/80-20/100 20/200 or worse
26 55 29 44 31
(14) (30) (16) (24) (16)
9 24 23 23 65
(6) (17) (16) (16) (45)
35 79 52 67 95
(11) (24) (16) (20) (29)
184
(100)
144
(100)
328
(100)
Rapidly developing nuclear sclerosis was noted as a complication by Michels5 in over one-third of the eyes in his series on epiretinal macular membrane stripping. When evaluating idiopathic cases with this complication in mind, 23 (12.5%) eyes had developed rapidly advancing nuclear sclerosis or rapidly increasing myopia. The mean age of these 23 eyes was 71.8 years, with a mean postoperative follow-up of 38 months. In order to evaluate the effect of cystoid macular edema on final visual outcome, preoperative fluorescein angiograms of the 184 idiopathic cases were graded independently by several experienced masked investigators, as to the presence and degree of cystoid macular edema. The grading went from zero in those eyes with no apparent edema to four plus in those eyes with four or more disc diameters of edema. Gradable angiograms were available in 150 of the 184 idiopathic operated eyes (Table 9). The gradings were then correlated with postoperative visual results and statistically evaluated: RHO 0.113, P = 0.1636; Tau = 0.018, P = 0.6844. In this series there was no relationship between the degree of preoperative cystoid macular edema and the final visual result. Pseudoholes or macular cysts were noted in 14 (8%) of the preoperative idiopathic eyes. The visual acuity ranged from 20/70 to C.F. in these eyes, 9 (60%) b~longing to females and 6 (40%) belonging to males, w1th a mean age of 61 years going from 32 to 71 years. Table 6. Visual Status Post-membrane Peeling in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membranes
All No.
Other
Visual Acuity
Total
Other
NUMBER 8
Table 5. Final Visual Outcome in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Peeling
Table 3. Etiologic Classification of 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane
Idiopathic Cases
•
Idiopathic Cases
Other
All
No. Eyes
No.
(%)
No.
(%)
No.
(%)
Improved (2 lines or more) Unchanged Worse
151 31 2
(82) (17) (1)
92 48 4
(64) (33) (3)
243 79 6
(74) (24) (2)
184
(100)
144
(100)
328
(100)
Total
MARGHERIO, et al
•
EPIMACULAR MEMBRANES
Table 8. Recurrence of Membrane in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Peeling
Table 7. Complications of 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Peeling Idiopathic (n = 184)
(n
Other = 144)
All (n
Complication
No.
(%)
No.
(%)
No.
(%}
Retinal detachment Retinal holes Endophthalmitis Rubeosis
2 0 1 0
(1) (0) (1) (0)
20 3 0 1
(14) (2) (0) (1)
22 3 1 1
(7) (1) (<1) (<1)
3
(2)
24
(17)
27
(8)
Total
Eyes with Recurrence
328)
=
Following membrane peeling these "pseudoholes" either markedly decreased in size or disappeared over a period of several weeks with correspondingly improved vision. Postoperative visual acuities ranged from 20/20 to 20/70 with an average improvement of five lines versus four lines in the idiopathic group as a whole.
DISCUSSION Epiretinal membranes proliferating on the inner retinal surface were probably first described by lwanoff in 1865.6 Through the years this clinical observation has gained more recognition, and in 1977 Foos 1 showed that the condition was relatively common in autopsied eyes, significantly increasing in incidence in older eyes from a rate of 2% at the age of 50 to over 20% at the age of 7 5. These membranes are composed of contractile cellular elements within a collagen matrix. 7 Because the median age of the population is increasing continually, the recognition and management of macular epiretinal membranes becomes more important. Macular epiretinal membranes may occur spontaneously (idiopathic) and are rarely congenital. They may also be associated with trauma, retinal reattachment surgery, photocoagulation or cryopexy, ocular inflammation, retinal vascular disease and vitreous hemorrhage. Macular epiretinal membranes may produce an alteration of the macular light reflex which has been likened
Etiology
Total
No.
(%)
Idiopathic Post-retinal detachment Retinal vascular Trauma Post-cryopexy, etc. Inflammation Congenital Congenital hereditary retinoschisis
11 4 4 2
184 95 13 12 11 10 2
(6) (4) (31) (17)
2
1 328
24
Total
(20) (100) 7.3
to the appearance of cellophane. In more advanced cases, the retinal wrinkling beneath the membrane is obvious by the distortion of the retinal vasculature with the larger vessels straightened and the smaller generally more tortuous and drawn to single or multiple epicenters (Fig l ). In some cases, the presence of a membrane cannot be appreciated except for this distortion of the retinal vasculature. In more advanced cases, the epiretinal tissue itself is sufficiently opaque to be visible by ophthalmoscopy and slit-lamp biomicroscopy. There may be associated intraretinal hemorrhages and edema, and occasionally the macula will appear cystic or may have the appearance of a macular hole or pseudohole (Fig 2). This appearance is enhanced with red-free ophthalmoscopy or photography. Fluorescein angiography may appear essentially normal except for the obvious distortion of the retinal vasculature. In many cases, however, with sufficient mechanical interference of the normal function of the retinal vessels, there is a breakdown of the blood-retina barrier with fluorescein leakage in the involved area and, occasionally, cystoid macular edema. Previous reports8 •9 suggest that this condition is nonprogressive. In this series, however, many patients were seen with initial visual acuities better than 20/70 and in follow-up examinations at six-month intervals, it was
Table 9. Influence of Preoperative Cystoid Macular Edema (CME) on Final Visual Acuity in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Lines of Visual Acuity Changed Degree of CME
0
0-1 1-2 2-3 3-4 4+
5 2
Total
9
2
3
4
5
6
7
8
Total
12 8 1 3 1
9 3 4 2 1
9 7 1 2 2
13 1 1 1 1
2 2 1 2
5 2 1 1
2
18 3 1 2 2
81 31 14 14 10
17
26
25
19
17
7
9
150
8 3 4
21
1079
OPHTHALMOLOGY
•
AUGUST 1985
•
VOLUME 92
•
NUMBER 8
Fig 1. Left, an idiopathic epiretinal membrane covers the macula with distortion of the underlying retinal vasculature. Right, fluorescein angiogram demonstrates distortion of retinal vessels leakage from perifoveal capillaries.
Fig 2. Left, an idiopathic epiretinal membrane with pseudohole in a 59-year-old man. Right, postoperative appearance after removal of intact thin membrane. Visual acuity improved from 20/100 to 20/30.
determined that this condition tended to be progressive, with further metamorphopsia and vision loss until the eyes became surgical candidates and were entered into the series. The rate of this progression was extremely variable, as demonstrated by one case that progressed from 20/50 to 20/200 over a period of seven years (Fig 3) while another patient deteriorated from 20/25 to counting fingers in less than three months (Fig 4). Both of these cases were classified as idiopathic. The surgical management of epiretinal macular membranes in nondiabetics was first introduced by Machemer in 197 8 10 and subsequently other authors reported favorable experiences with larger series. 11 - 14 Most of the subsequent reports, however, included a relatively small percentage of idiopathic or spontaneous cases. The results, therefore, were influenced by factors such as preexisting retinal detachments, vascular disorders, trauma, and inflammatory conditions. This article focuses on the idiopathic cases in an attempt to exclude as many extraneous influences as possible. 1080
In case selection, especially in the idiopathic or spontaneous variety, it must be emphasized that in many cases only a cellophane reflex with vascular tortuosity will be noted and no discrete membrane or edge will be visible. We would like to emphasize that it is not necessary to see a definite heavy membrane or edge to perform a successful membrane peeling and get a satisfactory surgical result. These cases may require somewhat more patience, but if performed in the suggested fashion, the complication rate is low and the success rate is high. Better visual results and a lower complication rate in the idiopathic group were expected since the idiopathic eyes generally had better visual potential due to the absence of previous retinal detachments, retinal vascular disease, etc. They were better surgical candidates since in the idiopathic group atrophic retinas, thick transvitreal membranes, high buckles, and other complicating factors were not present. Recurrences of epiretinal macular membranes were seen in 24 eyes (7.3%). The incidence in retinal vascular
MARGHERIO, et al
•
EPIMACULAR MEMBRANES
Fig 3. Left, An idiopathic epiretinal membrane in a 73-year-old man, November 1975. Visual acuity was 20/50. Right, appearance of fundus, October 1982. Visual acuity 20/200.
Fig 4. Left, An idiopathic epiretina1 membrane in a 71-year-old man, March 1983. Visual acuity was 20/25. Right, appearance in June 1983. Additional concentration of membrane with associated intraretinal hemorrhages and edema. Visual acuity count fingers.
(31% ), traumatic ( 17% ), and inflammatory (20%) cases was significantly higher and tended to occur in eyes with thick, opaque, vascularized membranes. Complete removal of all layers extending at least to the arcades and disc and 2 to 3 disc diameters temporal to the macula appeared to be important in reducing the incidence of recurrences. In some eyes it was virtually impossible to detect the presence of a second or third layer clinically, but oftentimes by using the previously described surgical technique, additional layers were identified and removed. Incomplete removal of portions of membranes or layers may account for "regrowth" in some cases. The rapid development of nuclear sclerosis following surgery for epiretinal macular membranes has been observed. This condition was noted in 12.5% of the idiopathic cases. This was a significantly lower incidence than in previously reported series. 5 •11 This can be explained in part by the lack of previous surgery in these eyes, especially scleral buckling procedures, which may have compromised the anterior segment with cryopexy,
diathermy, or encircling elements. Other possible factors influencing this discrepancy such as vitrectomy technique, distance of infusion port from the lens, type of irrigating fluid used, duration of procedures, and type of instrumentation have been previously reported. 15 The effect of preoperative cystoid macular edema on postoperative visual results in epiretinal macular membrane peelings is an area of controversy that has been raised by various authors. 13 • 14• 16 In this series, preoperative fluorescein angiograms suitable for grading were obtained in 150 of 184 idiopathic cases. A comparison of the gradings and final visual result demonstrated no relationship between the presence or degree of cystoid macular edema and the final visual result. Following successful membrane peeling the regression of the edema angiographically was variable. Macular cysts or pseudoholes were noted in 14 eyes, all in the idiopathic group of this series. To avoid rupture of the cyst, surgical technique varied slightly in these eyes. In performing the core vitrectomy care was 1081
OPHTHALMOLOGY •
AUGUST 1985 •
VOLUME 92 •
NUMBER 8
Fig 5. Left, thin idiopathic epiretinal membrane with macular pseudohole. Right, postoperative appearance with disappearance of macular pseudohole and improvement in visual acuity from 20/200 to 20/30.
taken to avoid traction on the macular region via the vitreomacular adhesions which were noted in 5 (35%) of the eyes as determined in the preoperative evaluation and substantiated at surgery. Care was taken during the membrane stripping to peel the membrane over the macula very slowly with tangential rather than AP traction. It was thought initially that these pseudoholes were part of the membrane as suggested by Allen and Gass. 17 However, in all 14 eyes the membranes were intact, and the pseudohole appeared to be a cystic lesion in the underlying neurosensory retina. The macular cyst or pseudohole was usually visible postoperatively for several weeks before decreasing in size or disappearing with subsequent improvement in vision (Fig 5). This observation may be important in the consideration of factors involved in the pathogenesis of macular cysts and holes. In the preoperative evaluation of eyes with pseudoholes, the use of the "slit beam" sign 3• 18 might identify cases with true macular holes where surgical intervention is probably not indicated.
REFERENCES
2.
3. 4. 5.
6.
7. 8.
9. 10.
11.
1. Foos RY. Surface wrinkling retinopathy. In: Freeman HM, Hirose T, Schepens CL, eds. Vitreous Surgery and Advances in Fundus
12.
Diagnosis and Treatment. New York: Appleton-Century-Crofts, 1977; 23-38. Clarkson JG, Green WR, Massof D. A histopathologic review of 168 cases of preretinal membrane. Am J Ophthalmol 1977; 84:117. Watzke RC, Allen L. Subjective slitbeam sign for macular disease. Am J Ophthalmol 1969; 68:449-53. Michels RG, Rice TA, Ober RR. Vitreoretinal dissection instruments. Am J Ophthalmol1979; 87:836-7. Michels RG. A clinical and histopathologic study of epiretinal membranes affecting the macula and removed by vitreous surgery. Trans Am Ophthalmol Soc 1982; 80:580-656. lwanoff A. Beitrii.ge zur normalen und pathologischen Anatomie des Auges. Albrecht von Graefes Arch Klin Exp Ophthalmol 1865; 11: 135-70. Trese M, Chandler DB, Machemer R. Macular pucker. II. Ultrastructure. Graefes Arch Clin Exp Ophthalmol 1983; 221:16-26. Gass JDM. Stereoscopic Atlas of Macular Disease; A Funduscopic and Angiographic Presentation. St Louis: CV Mosby, 1970; 20215. Sidd RJ, Fine SL, Owens SL, Patz A. Idiopathic preretinal gliosis. Am J Ophthalmol 1982; 94:44-8. Machemer R. Die chirurgische Entfernung von epiretinalen Makulamembranen (macular puckers). Klin Monatsbl Angenheilkd 1978; 173:36-42. Michels RG, Gilbert HD. Surgical management of macular pucker after retinal reattachment surgery. Am J Ophthalmol 1979; 88:925-9. Shea M. The surgical management of macular pucker. Can J Ophthalmol 1979; 14:110-3.
Discussion by C. P. Wilkinson, MD Idiopathic epimacular proliferation is a rather common, age-related condition 1 that is frequently misdiagnosed. These fibrocellular membranes reduce visual acuity by obscuring and detaching the macula and by distorting the retina and its blood From the Dean A. McGee Eye Institute and Department of Ophthalmology, University of Oklahoma Health Sciences Center.
1082
vessels. The authors have utilized closed vitrectomy techniques 2 in the surgical management of 184 idiopathic cases, and this number exceeds by many times the total number which have been reported in the literature. 3- 5 It should be emphasized that the eyes in this surgical series are not typical of routine cases of idiopathic epimacular proliferation. Visual acuities were 20/200 or less at the time of surgery in 73% of the series, and only 4% had 20/70 or
MARGHERIO, et al
•
better. These figures are quite different than those reported in consecutive nonsurgical series by Wise6 and by Sidd et aV in which 85% and 84% respectively presented with 20/70 vision or better. Although the authors have stated that many of their cases exhibited a significant progression of epimacular proliferation associated with visual acuity loss, the percentage of cases undergoing such changes was not stated. Such progression is frequently not the rule. In the series reported by Sidd et aV only 26% experienced two lines or more of visual acuity loss over a follow-up period averaging more than two and one half years. The anatomical and visual results in this series are impressive. The removal of idiopathic epimacular membranes was associated with an improvement in visual acuity of two lines or more in 82% of cases, a figure remarkably consistent to that presented by Michels5 at last year's American Academy. However, only 44% of eyes reached the 20/50 level or better, and patients should be advised that a return of normal visual acuity is quite unlikely. Although the authors have demonstrated that the degree of preoperative cystoid macular edema is not associated with a relatively poor prognosis, they were not able to identify other pre-operative factors which were associated significantly with either unexpectedly good or poor visual acuity results. In addition, the reasons that visions did not improve in 18% of idiopathic cases were not discussed. The complication rate of potentially blinding problems was low. Nuclear sclerosis following vitrectomy is an important problem which has been discussed by others, 5 and it was observed in 12.5% of these cases. Novak et al 8 have demonstrated in diabetic eyes undergoing vitrectomy that such postoperative nuclear lens changes are directly related to patient age. In this series, the mean age in cases in which nuclear lens changes developed was somewhat higher than that in the group as a whole, and it would be interesting to examine more thoroughly the precise statistical relationship between age and subsequent nuclear sclerosis. A precise relationship between clinical epimacular proliferation and responsible cell types observed histopathologically was not provided in this report. Most histopathological data9- 11 regarding idiopathic cases have implicated glial cells as responsible for membrane formation, and this was apparently true in this series. Nevertheless, a recent report by Michels3 demonstrated cell types that were not expected in idiopathic cases. In his small series, retinal pigment epithelial cells were involved in 60% of cases, whereas astrocytes were observed in only one of five specimens. Continued study of epiretinal membranes is of critical importance. It seems quite reasonable that epimacular proliferation may well represent a relatively localized form of a process related to massive proliferative vitreoretinopathy
EPIMACULAR MEMBRANES
(PVR), 12 the major cause of failure in retinal reattachment
surgery. Intraocular cellular proliferation and contraction represent a common problem leading to blindness, and this is observed not only in detachments with PVR but in traction and combined detachments following penetrating trauma. 13 •14 The authors have presented convincing data that, in skilled hands, closed vitrectomy techniques provide an effi~;ient and a relatively safe means of removing epimacular membranes. Further studies are needed both to define more precisely the preoperative factors associated with a good visual prognosis and to provide better explanations of the phenomenon of intraocular cellular proliferation and contraction. References 1. Roth AM, Foos RY. Surface wrinkling retinopathy in eyes enucleated at autopsy. Trans Am Acad Ophthalmol Otolaryngol1971; 75:104758. 2. Machemer R. A new concept for vitreous surgery. 7. Two instrument techniques in pars plana vitrectomy. Arch Ophthalmol 1974; 92: 407-12. 3. Michels RG. A clinical and histopathologic study of epiretinal membranes affecting the macula and removed by vitreous surgery. Trans Am Ophthalmol Soc 1982; 80:580-656. 4. Trese MT, Chandler DB, Machemer R. Macular pucker. I. Prognostic criteria. Graefes Arch Clin Exp Ophthalmol 1984; 221:12-5. 5. Michels RG. Vitrectomy for macular pucker. Ophthalmology 1984; 91:1384-7. 6. Wise GN. Clinical features of idiopathic preretinal macular fibrosis. Am J Ophthalmol 1975; 79:349-57. 7. Sidd RJ, Fine SL, Owens SL, Patz A. Idiopathic preretinal gliosis. Am J Ophthalmol 1982; 94:44-8. 8. Novak MA, Rice TA, Michels RG, Auer C. The crystalline lens after vitrectomy for diabetic retinopathy. 1984; 91:1480-4. 9. Bellhorn MB, Friedman AH, Wise GN, Henkind P. Ultrastructure and clinicopathologic correlation of idiopathic preretinal macular fibrosis. Am J Ophthalmol1975; 79:366-73. 10. Clarkson JG, Green WR, Masso! D. A histopathologic review of 168 cases of preretinal membrane. Am J Ophthalmol 1977; 84:1-
17. 11. Trese M, Chandler DB, Machemer R. Macular pucker. II. Ultrastructure. Graefes Arch Clin Exp Ophthalmol 1983; 221 :16-26. 12. The Retina Society Terminology Committee. The classification of retinal detachment with proliferative vitreoretinopathy. Ophthalmology 1983; 90:121-5. 13. Cleary PE, Ryan SJ. Histology of wound, vitreous, and retina in experimental posterior penetrating eye injury in the rhesus monkey. Am J Ophthalmol 1979; 88:221-31. 14. Ussmann JH, Lazarides E, Ryan SJ. Traction retinal detachment; a cell-mediated event. Arch Ophthalmol 1981; 99:869-72.
1083
Abstract: Vitreous surgery was used to remove epiretinal macular membranes in 328 cases, 184 (56%) of which had membranes that were considered idiopathic and 144 (44%) which were due to other causes. The 12- to 92month follow-up showed that visual acuity improved two lines or more in 243 (74%) of the eyes, 79 (24%) were unchanged and 6 (2%) became worse. Recurrence of membranes was seen in 24 (7.3%) eyes and 27 (8%) eyes developed complications. In the idiopathic cases visual results were significantly better and complications fewer. Rapidly progressive nuclear sclerosis was noted in 23 (12.5%) eyes. The degree of cystoid edema had no relationship to the final visual result. Pseudoholes which were present in 14 (8%) of the idiopathic cases either became smaller or disappeared following successful surgery with an average increase in acuity of five lines. [Key words: cystoid macular edema, epiretinal macular membranes, macular cyst, macular pucker, preretinal macular fibrosis, primary retinal folds, pseudohole of the macula, surface wrinkling retinopathy, vitrectomy, vitreous surgery.] Ophthalmology 92:1075-1083, 1985
Cellular membranes on the inner retinal surface are common. They have occurred in 2 to 6% of autopsied eyes having an increasing incidence with age. 1•2 Most spontaneous or idiopathic membranes cause minor visual disturbances and are slowly progressive, while some membranes cause progressive metamorphopsia, Amsler grid distortion, and reduced visual acuity due to distortion and/or obscuration of the macula. The macular distortion produced by epiretinal membranes has been called primary retinal folds, macular pucker, preretinal macular fibrosis, surface wrinkling retinopathy, preretinal macular fibrosis, internal-retinal fibrosis, and cellophane maculopathy. The condition is commonly called a macular pucker when it follows the surgical reattachment of a rhegmatogenous retinal detachment. From the Division of Ophthalmology, Michigan State University, College of Human Medicine, East Lansing, Michigan, and the Department of Ophthalmology, William Beaumont Hospital, Royal Oak, Michigan. Presented at the Eighty-ninth Annual Meeting of the American Academy of Ophthalmology, Atlanta, Georgia, November 11-15, 1984. Reprint requests to Raymond R. Margherio, MD, 3535 W. 13 Mile Road, Suite 507, Royal Oak, Ml 48072.
In this series, the results of a long-term study of 328 affected eyes that have undergone vitrectomy with epiretinal membrane peeling will be reported. Of the 328 eyes, 184 were considered to be idiopathic or spontaneous, and although this series reports on all types of etiologically identified epiretinal macular membranes, particular emphasis is placed on idiopathic epiretinal membranes rather than macular puckers following retinal surgery. An attempt is made to identify some of the prognostic factors that may affect the selection of patients for possible surgical intervention, including thickness of membrane, presence of a visible edge, location of membrane, preoperative cystoid macular edema, and presence of a macular cyst or pseudohole. Surgical technique is discussed with comments regarding avoidance of complications and ways of dealing with unusual case types.
MATERIALS AND METHODS All patients were operated on by a member of Associated Retinal Consultants in Royal Oak, Michigan between April 1977 and October 1983. The patients were generally referred for evaluation with a diagnosis 1075
OPHTHALMOLOGY
•
AUGUST 1985
of macular degeneration. Eyes exhibiting epiretinal macular membranes were sub-classified based on presumed etiology. Eyes with any evidence of diabetic retinopathy, senile macular degeneration, glaucoma with field loss, previous retinal detachments involving the macula, or with significant opacities of the ocular media were excluded. A complete eye examination was performed on all eyes preoperatively. In addition, a comprehensive evaluation of the vitreous was performed with a contact lens. Stereo fundus photographs were taken and fluorescein angiography was performed when possible. In eyes with an apparent macular cyst, hole, or pseudohole, the "slit beam sign" 3 was used. In performing the slit beam test, a narrow beam of light is directed over the macula. The presence of a macular hole or large cyst causes the patient to report a discontinuous line or gap in the beam, whereas small cysts or pseudoholes cause the light to be pinched in appearance. Other lesions, such as detachments of the neurosensory retina, cause a bowing of the slit. In this study, a "positive" response was when a patient described the slit as being discontinuous. Eyes with positive "slit beam signs" were not considered favorable surgical candidates. Initially, no eye was considered for surgery with a corrected vision of better than 20/200. As the surgical technique was improved, and detailed analysis showed that the procedure was relatively safe and usually effective, this parameter was lowered to approximately 20/ 70 on selected patients. However, the vast majority of patients considered for surgery had corrected visual acuities that were less than 20/200. Many patients were seen with epiretinal macular membranes and visual acuities better than 20/70. These patients were given an Amsler grid and examined, generally, at six-month intervals. Statistical analyses were done using an Apple II C Computer Statistics Package. Two nonparametric tests were performed. The first was the Spearman rank-order coefficient rs (rho) which tests the relationships between two variables by assigning rank orders and then computing the differences between the ranks and squaring the differences (to eliminate signs). The second was the Kendall Tau (T) which looks at data by performing pairwise comparisons between one pair of values and all other lower ranking pairs.
SURGICAL OBJECTIVES AND TECHNIQUES The initial surgical objective in these cases was to perform a core vitrectomy, utilizing either a full function vitrector or divided system vitrectomy instrumentation. A bimanual technique was used for the membrane stripping, generally with a full function vitrectomy instrument entering the globe superior temporally and a bent needle superior nasally. A 23-gauge 1112 inch dis-
1076
•
VOLUME 92
•
NUMBER 8
posable needle attached to a tuberculin syringe filled with a balanced salt solution is most convenient for the procedure. Prior to bending, the needle is inserted into the vitreous cavity through the pars plana. Any sclera, etc., is then irrigated out of the bore and an appropriate bend is made near the tip under the microscope. The needle can then easily be reinserted into the globe through the self-sealing puncture wound, which can later be closed with a single suture. In cases where forceps or scissors may be required, this nasal inci!Sion is made with an appropriate knife or stylet. Approximately one-half of the eyes of this series were operated on with a full function instrument and one-half using a divided system. Prior to attempting the membrane peeling, the posterior one-half of the globe must be free of vitreous. This was easily accomplished in most of the eyes in this series with a posterior vitreous detachment present preoperatively. In the remainder of the eyes, without a posterior vitreous detachment, a complete posterior vitrectomy was necessary to remove all vitreous opacities, thereby improving visualization and reducing the possibility of peripheral vitreoretinal traction that could cause retinal tears or detachment. In performing the core vitrectomy, an attempt was made to leave as much vitreous between the core vitrectomy and the lens as possible in an attempt to reduce the possibility of trauma to the lens, and hopefully, the incidence of postoperative cataract formation. Following the core vitrectomy, a bent 23-gauge needle or vitreoretinal pick4 was used to strip away the epiretinal tissue in order to allow the retina to assume a more normal configuration. In a minority of cases the epiretinal tissue itself was opaque, causing additional interference with clear vision. The manner in which the core vitrectomy was achieved varied with each case, depending on multiple factors determined by careful preoperative evaluation. These factors included the presence of a lens or pseudophakos, previous retinal reattachment surgery, transvitreal bands, preexisting retinal tears or subclinical detachments, atrophic or nonprofused retina, presence of a macular cyst or pseudohole, and the clinical appearance and position of the epiretinal membrane. Of the aforementioned considerations, eyes with transvitreal membranes, usually associated with previous retinal detachments, were technically the most difficult. Also, eyes that had previous scleral buckling procedures with very high buckles had to be approached in such a way that the shafts of the instruments would pass from the pars plana to the paramacular region with enough clearance over the buckle to avoid tearing the retina during dissection. In cases where retinal tears or subclinical detachments were noted, the retinal repair was carried out at least three months prior to any attempt at vitrectomy and removal of surgical epiretinal membranes. There were no subsequent detachments in eyes treated in this fashion. In almost all cases the membrane itself was first
MARGHERIO,
et al •
dissected with a bent 23-gauge needle. If the membrane demonstrated an obvious edge this was dissected first. If not, the area of greatest apparent thickness or tortuosity was dissected using the sharp point of the needle over one of the minor retinal vessels in an attempt to find an edge. When using this technique, a small intraretinal bleed was noted before a full thickness perforation occurred during the dissection. In cases where there was no edge, obvious thickening, or epicenter, the same technique was used in multiple areas until an edge was encountered, which then allowed successful stripping of the membrane. In cases where atrophic retina, due to trauma or vascular occlusive disease, etc., was identified, more care was necessary in all phases of the membrane stripping, since these retinas did not exhibit the same amount of tensile strength and were more apt to tear with the membrane stripping than a retina not so compromised. Special care was taken when stripping the membrane over the macula, especially in cases where there was a pseudohole or cyst in order to avoid creating a lamellar or true macular hole. This complication was not encountered in this series, but has been seen in several eyes undergoing membrane stripping for diabetic retinopathy. In most cases, the membrane was removed starting from an area two to three disc diameters temporal to the macula and proceeding towards the disc nasally and the arcades inferiorly and superiorly, removing as much intact membrane as possible. In cases where a specimen was desired for histopathologic study or where the edge of the membrane could not be grasped with the needle for dissection, intravitreal forceps were used. Care was taken during the dissection phase to observe all areas of potential traction so that retinal tears were not created. In some cases the membrane peeled and became very extensive, going far beyond the arcades. In these cases it was very difficult to observe all areas of traction and it was felt these membranes should be cut circumferentially with intravitreal scissors to reduce the possibility of retinal tears and/or detachment. In peeling almost all cases of idiopathic membranes, which were generally thin and transparent, the bent 23-gauge needl~ was the instrument of choice. Where thick, however, opaque membranes were encountered with large convolutions of retina, a vitreoretinal pick with a more blunt tip was useful to separate the membrane from the retina and was less likely to cause a retinal break especially in some cases of macular pucker after a scleral buckling procedure where often a "plug" of fibrous material had to be removed from the "epicenter" of the pucker if visual improvement was to occur. With thin transparent membranes there is generally no need to search for multiple layered membranes. However, with thicker, more opaque membranes there are often multiple layers that must be sequentially peeled in order to obtain the desired end point. In most instances, by using the previously noted technique of careful dissection over small vessels until encountering capillary bleeding, incomplete removal of multilayered
EPIMACULAR MEMBRANES
Table 1. Age Distribution in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Idiopathic Cases
Other
All
21-86 67.8
5-83 54.3 57
5-86 60.67 65
Range (years) Mean (years) Median (years)
69
membranes can be avoided. However, since the eyes that had an air-fluid exchange were not selected in a randomized fashion, a statistical analysis of the effects on final visual outcome was not significant. Any retinal tears created during the vitrectomy or stripping were treated with trans-scleral cryopexy, transvitreal cryopexy, or photocoagulation. In cases where there was a great deal of folding of the retina, it was felt that an air-fluid exchange and postoperative prone positioning of the patient might result in a better anatomic result. This was done in approximately one-half of the cases in this series.
RESULTS The age of the patients in this study ranged from 5 to 86 years (mean, 60.67 years) (Table 1). The idiopathic group were generally older with a mean of 67.8 years, which would be consistent with the findings of Foos and others 1•2 regarding incidence, etc. There were 140 males and 188 females, with a marked prevalence of females in the idiopathic group and a slight prevalence of males in the other category (Table 2). The most common type of macular membrane was spontaneous or idiopathic. Membranes following retinal reattachment were the second most common type. The membranes were also seen following the prophylactic treatment of retinal breaks, trauma, ocular inflammation and retinal vascular diseases. Two membranes were considered to be congenital in origin and one was associated with juvenile sex-linked retinoschisis (Table 3). The follow-up period after the removal of the epiretinal macular membranes from the 328 eyes ranged from 12 months to 92 months (mean, 41.2 months). The best preoperative visual acuity was 20/60. In most eyes the Table 2. Sex Distribution in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Idiopathic Cases
All
Other
No.
(%)
No.
(%)
No.
(%)
Male Female
63 121
(34) (66)
77
67
(53) (47)
140 188
(43) (57)
Total
184
(100)
144
(100)
328
(100)
1077
OPHTHALMOLOGY
•
AUGUST 1985
•
VOLUME 92
Condition
No.
(%)
Idiopathic Post-retinal detachment Retinal vascular Trauma Post-cryopexy, photocoagulation, etc. Inflammatory Congenital Congenital hereditary retinoschisis
184 95 13 12 11 10 2 1
(56) (29) (4) (4) (3) (3) (0.7) (0.3)
Idiopathic Cases
preoperative visual acuity was 20/200 or worse (Table 4). Economically useful vision (20/50 or better) was restored in approximately one-third (34%) of the operated eyes (Table 5). Forty-four percent of the eyes with idiopathic membranes achieved a visual acuity of 20/50 or better. Similar visual results were obtained in only 23% of eyes with membranes due to other causes. The average number oflines of improvement of visual acuity following macular membrane peeling was 3.45. The results again being better in the idiopathic cases (4.03 lines) versus the other cases (2.99 lines). Over all the visual acuity improved two lines or more in approximately 74% of the operated eyes. Twenty-four percent were unchanged and visual acuity was worse in 2% of the 328 eyes operated (Table 6). Twenty-seven eyes developed complications following surgery. The vast majority of these complications related to the recurrence of a retinal detachment in eyes with scleral buckles in place. These were all successfully repaired. The one case of endophthalmitis was also successfully treated. In the series of idiopathic cases the~e was a complication rate of approximately 2%, wh1ch was much lower than the overall complication rate of 8% (Table 7). Recurrence of epiretinal membranes was observed in 24 (7.3%) eyes. Recurrence was relatively infrequent except in younger patients and in eyes with membranes associated with retinovascular conditions (31% ), inflammation (20%) and trauma ( 17%) (Table 8). Table 4. Visual Acuity in 328 Consecutive Cases of Vitrectomy for Ep1ret1nal Macular Membrane Prior to Membrane Peeling
Visual Acuity 20/20-20/30 20/40-20/50 20/60-20/70 20/80-20/100 20/200 or worse Total
1078
No.
(%)
No.
(%)
(%)
(2 (15) (83) (100)
7 43 134
(4) (23) (73)
5 139
(3) (97)
7 48 273
184
(100)
144
(100)
328
All
No.
(%)
No.
(%)
No.
(%)
20/20-20/30 20/40-20/50 20/60-20/70 20/80-20/100 20/200 or worse
26 55 29 44 31
(14) (30) (16) (24) (16)
9 24 23 23 65
(6) (17) (16) (16) (45)
35 79 52 67 95
(11) (24) (16) (20) (29)
184
(100)
144
(100)
328
(100)
Rapidly developing nuclear sclerosis was noted as a complication by Michels5 in over one-third of the eyes in his series on epiretinal macular membrane stripping. When evaluating idiopathic cases with this complication in mind, 23 (12.5%) eyes had developed rapidly advancing nuclear sclerosis or rapidly increasing myopia. The mean age of these 23 eyes was 71.8 years, with a mean postoperative follow-up of 38 months. In order to evaluate the effect of cystoid macular edema on final visual outcome, preoperative fluorescein angiograms of the 184 idiopathic cases were graded independently by several experienced masked investigators, as to the presence and degree of cystoid macular edema. The grading went from zero in those eyes with no apparent edema to four plus in those eyes with four or more disc diameters of edema. Gradable angiograms were available in 150 of the 184 idiopathic operated eyes (Table 9). The gradings were then correlated with postoperative visual results and statistically evaluated: RHO 0.113, P = 0.1636; Tau = 0.018, P = 0.6844. In this series there was no relationship between the degree of preoperative cystoid macular edema and the final visual result. Pseudoholes or macular cysts were noted in 14 (8%) of the preoperative idiopathic eyes. The visual acuity ranged from 20/70 to C.F. in these eyes, 9 (60%) b~longing to females and 6 (40%) belonging to males, w1th a mean age of 61 years going from 32 to 71 years. Table 6. Visual Status Post-membrane Peeling in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membranes
All No.
Other
Visual Acuity
Total
Other
NUMBER 8
Table 5. Final Visual Outcome in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Peeling
Table 3. Etiologic Classification of 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane
Idiopathic Cases
•
Idiopathic Cases
Other
All
No. Eyes
No.
(%)
No.
(%)
No.
(%)
Improved (2 lines or more) Unchanged Worse
151 31 2
(82) (17) (1)
92 48 4
(64) (33) (3)
243 79 6
(74) (24) (2)
184
(100)
144
(100)
328
(100)
Total
MARGHERIO, et al
•
EPIMACULAR MEMBRANES
Table 8. Recurrence of Membrane in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Peeling
Table 7. Complications of 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Peeling Idiopathic (n = 184)
(n
Other = 144)
All (n
Complication
No.
(%)
No.
(%)
No.
(%}
Retinal detachment Retinal holes Endophthalmitis Rubeosis
2 0 1 0
(1) (0) (1) (0)
20 3 0 1
(14) (2) (0) (1)
22 3 1 1
(7) (1) (<1) (<1)
3
(2)
24
(17)
27
(8)
Total
Eyes with Recurrence
328)
=
Following membrane peeling these "pseudoholes" either markedly decreased in size or disappeared over a period of several weeks with correspondingly improved vision. Postoperative visual acuities ranged from 20/20 to 20/70 with an average improvement of five lines versus four lines in the idiopathic group as a whole.
DISCUSSION Epiretinal membranes proliferating on the inner retinal surface were probably first described by lwanoff in 1865.6 Through the years this clinical observation has gained more recognition, and in 1977 Foos 1 showed that the condition was relatively common in autopsied eyes, significantly increasing in incidence in older eyes from a rate of 2% at the age of 50 to over 20% at the age of 7 5. These membranes are composed of contractile cellular elements within a collagen matrix. 7 Because the median age of the population is increasing continually, the recognition and management of macular epiretinal membranes becomes more important. Macular epiretinal membranes may occur spontaneously (idiopathic) and are rarely congenital. They may also be associated with trauma, retinal reattachment surgery, photocoagulation or cryopexy, ocular inflammation, retinal vascular disease and vitreous hemorrhage. Macular epiretinal membranes may produce an alteration of the macular light reflex which has been likened
Etiology
Total
No.
(%)
Idiopathic Post-retinal detachment Retinal vascular Trauma Post-cryopexy, etc. Inflammation Congenital Congenital hereditary retinoschisis
11 4 4 2
184 95 13 12 11 10 2
(6) (4) (31) (17)
2
1 328
24
Total
(20) (100) 7.3
to the appearance of cellophane. In more advanced cases, the retinal wrinkling beneath the membrane is obvious by the distortion of the retinal vasculature with the larger vessels straightened and the smaller generally more tortuous and drawn to single or multiple epicenters (Fig l ). In some cases, the presence of a membrane cannot be appreciated except for this distortion of the retinal vasculature. In more advanced cases, the epiretinal tissue itself is sufficiently opaque to be visible by ophthalmoscopy and slit-lamp biomicroscopy. There may be associated intraretinal hemorrhages and edema, and occasionally the macula will appear cystic or may have the appearance of a macular hole or pseudohole (Fig 2). This appearance is enhanced with red-free ophthalmoscopy or photography. Fluorescein angiography may appear essentially normal except for the obvious distortion of the retinal vasculature. In many cases, however, with sufficient mechanical interference of the normal function of the retinal vessels, there is a breakdown of the blood-retina barrier with fluorescein leakage in the involved area and, occasionally, cystoid macular edema. Previous reports8 •9 suggest that this condition is nonprogressive. In this series, however, many patients were seen with initial visual acuities better than 20/70 and in follow-up examinations at six-month intervals, it was
Table 9. Influence of Preoperative Cystoid Macular Edema (CME) on Final Visual Acuity in 328 Consecutive Cases of Vitrectomy for Epiretinal Macular Membrane Lines of Visual Acuity Changed Degree of CME
0
0-1 1-2 2-3 3-4 4+
5 2
Total
9
2
3
4
5
6
7
8
Total
12 8 1 3 1
9 3 4 2 1
9 7 1 2 2
13 1 1 1 1
2 2 1 2
5 2 1 1
2
18 3 1 2 2
81 31 14 14 10
17
26
25
19
17
7
9
150
8 3 4
21
1079
OPHTHALMOLOGY
•
AUGUST 1985
•
VOLUME 92
•
NUMBER 8
Fig 1. Left, an idiopathic epiretinal membrane covers the macula with distortion of the underlying retinal vasculature. Right, fluorescein angiogram demonstrates distortion of retinal vessels leakage from perifoveal capillaries.
Fig 2. Left, an idiopathic epiretinal membrane with pseudohole in a 59-year-old man. Right, postoperative appearance after removal of intact thin membrane. Visual acuity improved from 20/100 to 20/30.
determined that this condition tended to be progressive, with further metamorphopsia and vision loss until the eyes became surgical candidates and were entered into the series. The rate of this progression was extremely variable, as demonstrated by one case that progressed from 20/50 to 20/200 over a period of seven years (Fig 3) while another patient deteriorated from 20/25 to counting fingers in less than three months (Fig 4). Both of these cases were classified as idiopathic. The surgical management of epiretinal macular membranes in nondiabetics was first introduced by Machemer in 197 8 10 and subsequently other authors reported favorable experiences with larger series. 11 - 14 Most of the subsequent reports, however, included a relatively small percentage of idiopathic or spontaneous cases. The results, therefore, were influenced by factors such as preexisting retinal detachments, vascular disorders, trauma, and inflammatory conditions. This article focuses on the idiopathic cases in an attempt to exclude as many extraneous influences as possible. 1080
In case selection, especially in the idiopathic or spontaneous variety, it must be emphasized that in many cases only a cellophane reflex with vascular tortuosity will be noted and no discrete membrane or edge will be visible. We would like to emphasize that it is not necessary to see a definite heavy membrane or edge to perform a successful membrane peeling and get a satisfactory surgical result. These cases may require somewhat more patience, but if performed in the suggested fashion, the complication rate is low and the success rate is high. Better visual results and a lower complication rate in the idiopathic group were expected since the idiopathic eyes generally had better visual potential due to the absence of previous retinal detachments, retinal vascular disease, etc. They were better surgical candidates since in the idiopathic group atrophic retinas, thick transvitreal membranes, high buckles, and other complicating factors were not present. Recurrences of epiretinal macular membranes were seen in 24 eyes (7.3%). The incidence in retinal vascular
MARGHERIO, et al
•
EPIMACULAR MEMBRANES
Fig 3. Left, An idiopathic epiretinal membrane in a 73-year-old man, November 1975. Visual acuity was 20/50. Right, appearance of fundus, October 1982. Visual acuity 20/200.
Fig 4. Left, An idiopathic epiretina1 membrane in a 71-year-old man, March 1983. Visual acuity was 20/25. Right, appearance in June 1983. Additional concentration of membrane with associated intraretinal hemorrhages and edema. Visual acuity count fingers.
(31% ), traumatic ( 17% ), and inflammatory (20%) cases was significantly higher and tended to occur in eyes with thick, opaque, vascularized membranes. Complete removal of all layers extending at least to the arcades and disc and 2 to 3 disc diameters temporal to the macula appeared to be important in reducing the incidence of recurrences. In some eyes it was virtually impossible to detect the presence of a second or third layer clinically, but oftentimes by using the previously described surgical technique, additional layers were identified and removed. Incomplete removal of portions of membranes or layers may account for "regrowth" in some cases. The rapid development of nuclear sclerosis following surgery for epiretinal macular membranes has been observed. This condition was noted in 12.5% of the idiopathic cases. This was a significantly lower incidence than in previously reported series. 5 •11 This can be explained in part by the lack of previous surgery in these eyes, especially scleral buckling procedures, which may have compromised the anterior segment with cryopexy,
diathermy, or encircling elements. Other possible factors influencing this discrepancy such as vitrectomy technique, distance of infusion port from the lens, type of irrigating fluid used, duration of procedures, and type of instrumentation have been previously reported. 15 The effect of preoperative cystoid macular edema on postoperative visual results in epiretinal macular membrane peelings is an area of controversy that has been raised by various authors. 13 • 14• 16 In this series, preoperative fluorescein angiograms suitable for grading were obtained in 150 of 184 idiopathic cases. A comparison of the gradings and final visual result demonstrated no relationship between the presence or degree of cystoid macular edema and the final visual result. Following successful membrane peeling the regression of the edema angiographically was variable. Macular cysts or pseudoholes were noted in 14 eyes, all in the idiopathic group of this series. To avoid rupture of the cyst, surgical technique varied slightly in these eyes. In performing the core vitrectomy care was 1081
OPHTHALMOLOGY •
AUGUST 1985 •
VOLUME 92 •
NUMBER 8
Fig 5. Left, thin idiopathic epiretinal membrane with macular pseudohole. Right, postoperative appearance with disappearance of macular pseudohole and improvement in visual acuity from 20/200 to 20/30.
taken to avoid traction on the macular region via the vitreomacular adhesions which were noted in 5 (35%) of the eyes as determined in the preoperative evaluation and substantiated at surgery. Care was taken during the membrane stripping to peel the membrane over the macula very slowly with tangential rather than AP traction. It was thought initially that these pseudoholes were part of the membrane as suggested by Allen and Gass. 17 However, in all 14 eyes the membranes were intact, and the pseudohole appeared to be a cystic lesion in the underlying neurosensory retina. The macular cyst or pseudohole was usually visible postoperatively for several weeks before decreasing in size or disappearing with subsequent improvement in vision (Fig 5). This observation may be important in the consideration of factors involved in the pathogenesis of macular cysts and holes. In the preoperative evaluation of eyes with pseudoholes, the use of the "slit beam" sign 3• 18 might identify cases with true macular holes where surgical intervention is probably not indicated.
REFERENCES
2.
3. 4. 5.
6.
7. 8.
9. 10.
11.
1. Foos RY. Surface wrinkling retinopathy. In: Freeman HM, Hirose T, Schepens CL, eds. Vitreous Surgery and Advances in Fundus
12.
Diagnosis and Treatment. New York: Appleton-Century-Crofts, 1977; 23-38. Clarkson JG, Green WR, Massof D. A histopathologic review of 168 cases of preretinal membrane. Am J Ophthalmol 1977; 84:117. Watzke RC, Allen L. Subjective slitbeam sign for macular disease. Am J Ophthalmol 1969; 68:449-53. Michels RG, Rice TA, Ober RR. Vitreoretinal dissection instruments. Am J Ophthalmol1979; 87:836-7. Michels RG. A clinical and histopathologic study of epiretinal membranes affecting the macula and removed by vitreous surgery. Trans Am Ophthalmol Soc 1982; 80:580-656. lwanoff A. Beitrii.ge zur normalen und pathologischen Anatomie des Auges. Albrecht von Graefes Arch Klin Exp Ophthalmol 1865; 11: 135-70. Trese M, Chandler DB, Machemer R. Macular pucker. II. Ultrastructure. Graefes Arch Clin Exp Ophthalmol 1983; 221:16-26. Gass JDM. Stereoscopic Atlas of Macular Disease; A Funduscopic and Angiographic Presentation. St Louis: CV Mosby, 1970; 20215. Sidd RJ, Fine SL, Owens SL, Patz A. Idiopathic preretinal gliosis. Am J Ophthalmol 1982; 94:44-8. Machemer R. Die chirurgische Entfernung von epiretinalen Makulamembranen (macular puckers). Klin Monatsbl Angenheilkd 1978; 173:36-42. Michels RG, Gilbert HD. Surgical management of macular pucker after retinal reattachment surgery. Am J Ophthalmol 1979; 88:925-9. Shea M. The surgical management of macular pucker. Can J Ophthalmol 1979; 14:110-3.
Discussion by C. P. Wilkinson, MD Idiopathic epimacular proliferation is a rather common, age-related condition 1 that is frequently misdiagnosed. These fibrocellular membranes reduce visual acuity by obscuring and detaching the macula and by distorting the retina and its blood From the Dean A. McGee Eye Institute and Department of Ophthalmology, University of Oklahoma Health Sciences Center.
1082
vessels. The authors have utilized closed vitrectomy techniques 2 in the surgical management of 184 idiopathic cases, and this number exceeds by many times the total number which have been reported in the literature. 3- 5 It should be emphasized that the eyes in this surgical series are not typical of routine cases of idiopathic epimacular proliferation. Visual acuities were 20/200 or less at the time of surgery in 73% of the series, and only 4% had 20/70 or
MARGHERIO, et al
•
better. These figures are quite different than those reported in consecutive nonsurgical series by Wise6 and by Sidd et aV in which 85% and 84% respectively presented with 20/70 vision or better. Although the authors have stated that many of their cases exhibited a significant progression of epimacular proliferation associated with visual acuity loss, the percentage of cases undergoing such changes was not stated. Such progression is frequently not the rule. In the series reported by Sidd et aV only 26% experienced two lines or more of visual acuity loss over a follow-up period averaging more than two and one half years. The anatomical and visual results in this series are impressive. The removal of idiopathic epimacular membranes was associated with an improvement in visual acuity of two lines or more in 82% of cases, a figure remarkably consistent to that presented by Michels5 at last year's American Academy. However, only 44% of eyes reached the 20/50 level or better, and patients should be advised that a return of normal visual acuity is quite unlikely. Although the authors have demonstrated that the degree of preoperative cystoid macular edema is not associated with a relatively poor prognosis, they were not able to identify other pre-operative factors which were associated significantly with either unexpectedly good or poor visual acuity results. In addition, the reasons that visions did not improve in 18% of idiopathic cases were not discussed. The complication rate of potentially blinding problems was low. Nuclear sclerosis following vitrectomy is an important problem which has been discussed by others, 5 and it was observed in 12.5% of these cases. Novak et al 8 have demonstrated in diabetic eyes undergoing vitrectomy that such postoperative nuclear lens changes are directly related to patient age. In this series, the mean age in cases in which nuclear lens changes developed was somewhat higher than that in the group as a whole, and it would be interesting to examine more thoroughly the precise statistical relationship between age and subsequent nuclear sclerosis. A precise relationship between clinical epimacular proliferation and responsible cell types observed histopathologically was not provided in this report. Most histopathological data9- 11 regarding idiopathic cases have implicated glial cells as responsible for membrane formation, and this was apparently true in this series. Nevertheless, a recent report by Michels3 demonstrated cell types that were not expected in idiopathic cases. In his small series, retinal pigment epithelial cells were involved in 60% of cases, whereas astrocytes were observed in only one of five specimens. Continued study of epiretinal membranes is of critical importance. It seems quite reasonable that epimacular proliferation may well represent a relatively localized form of a process related to massive proliferative vitreoretinopathy
EPIMACULAR MEMBRANES
(PVR), 12 the major cause of failure in retinal reattachment
surgery. Intraocular cellular proliferation and contraction represent a common problem leading to blindness, and this is observed not only in detachments with PVR but in traction and combined detachments following penetrating trauma. 13 •14 The authors have presented convincing data that, in skilled hands, closed vitrectomy techniques provide an effi~;ient and a relatively safe means of removing epimacular membranes. Further studies are needed both to define more precisely the preoperative factors associated with a good visual prognosis and to provide better explanations of the phenomenon of intraocular cellular proliferation and contraction. References 1. Roth AM, Foos RY. Surface wrinkling retinopathy in eyes enucleated at autopsy. Trans Am Acad Ophthalmol Otolaryngol1971; 75:104758. 2. Machemer R. A new concept for vitreous surgery. 7. Two instrument techniques in pars plana vitrectomy. Arch Ophthalmol 1974; 92: 407-12. 3. Michels RG. A clinical and histopathologic study of epiretinal membranes affecting the macula and removed by vitreous surgery. Trans Am Ophthalmol Soc 1982; 80:580-656. 4. Trese MT, Chandler DB, Machemer R. Macular pucker. I. Prognostic criteria. Graefes Arch Clin Exp Ophthalmol 1984; 221:12-5. 5. Michels RG. Vitrectomy for macular pucker. Ophthalmology 1984; 91:1384-7. 6. Wise GN. Clinical features of idiopathic preretinal macular fibrosis. Am J Ophthalmol 1975; 79:349-57. 7. Sidd RJ, Fine SL, Owens SL, Patz A. Idiopathic preretinal gliosis. Am J Ophthalmol 1982; 94:44-8. 8. Novak MA, Rice TA, Michels RG, Auer C. The crystalline lens after vitrectomy for diabetic retinopathy. 1984; 91:1480-4. 9. Bellhorn MB, Friedman AH, Wise GN, Henkind P. Ultrastructure and clinicopathologic correlation of idiopathic preretinal macular fibrosis. Am J Ophthalmol1975; 79:366-73. 10. Clarkson JG, Green WR, Masso! D. A histopathologic review of 168 cases of preretinal membrane. Am J Ophthalmol 1977; 84:1-
17. 11. Trese M, Chandler DB, Machemer R. Macular pucker. II. Ultrastructure. Graefes Arch Clin Exp Ophthalmol 1983; 221 :16-26. 12. The Retina Society Terminology Committee. The classification of retinal detachment with proliferative vitreoretinopathy. Ophthalmology 1983; 90:121-5. 13. Cleary PE, Ryan SJ. Histology of wound, vitreous, and retina in experimental posterior penetrating eye injury in the rhesus monkey. Am J Ophthalmol 1979; 88:221-31. 14. Ussmann JH, Lazarides E, Ryan SJ. Traction retinal detachment; a cell-mediated event. Arch Ophthalmol 1981; 99:869-72.
1083